Haverford College
Haverford Scholarship
Faculty Publications
Biology
2013
Modeling 400 million years of plant hydraulics
Jonathan P. Wilson
Haverford College, [email protected]
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Repository Citation
Wilson, J. P., 2013, Modeling 400 million years of plant hydraulics: The Paleontological Society Papers, v. 19, p. 175-194.
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MODELING 400 MILLION YEARS OF PLANT HYDRAULICS
JONATHAN P. WILSON
Department of Biology, Haverford College, 370 Lancaster Ave., Haverford, PA 19041 USA
<[email protected]>
ABSTRACT.—Mathematical models of fluid flow thorough plant stems permit quantitative assessment of
plant ecology using anatomy alone, allowing extinct and extant plants to be measured against one another.
Through this process, a series of patterns and observations about plant ecology and evolution can be
made. First, many plants evolved high rates of water transport through the evolution of a diverse suite of
anatomical adaptations over the last four hundred million years. Second, adaptations to increase hydraulic
supply to leaves tend to precede, in evolutionary time, adaptations to increase the safety margin of plant
water transport. Third, anatomical breakthroughs in water transport function tend to occur in step with
ecological breakthroughs, including the appearance of leaves during the Devonian, the evolution of high
leaf areas in early seed plants during the Carboniferous, and the early radiation of flowering plants during
the Cretaceous. Quantitative assessment of plant function not only opens up the plant fossil record to
ecological comparison, but also provides data that can be used to model fluxes and dynamics of past
ecosystems that are rooted in individual plant anatomy.
INTRODUCTION
The biophysical nature of plant physiology means
that functional and ecological insights can be
derived from plant anatomy and morphology.
More than one hundred and fifty years of work on
living and fossil plants (Brongniart, 1828; Bailey
and Sinnott, 1915; Bailey and Sinnott, 1916) has
aimed to understand not only the environments
these plants inhabited (Arens et al., 2000;
Beerling and Royer, 2002a, b; Kohn and
Thiemens, 2010), but also the evolutionary
trajectory of terrestrial plant function. Key aspects
of plant physiology are determined by the
physical properties of individual plant cells, and
these dimensions can be preserved in the fossil
record, opening up the evolutionary history of
land plants’ physiology to analysis. Recent work
applying mathematical models to key plant
tissues, namely water transport cells, has opened
the door to quantitative understanding of the 400million-year evolutionary history of vascular
plants (Cichan 1986a; Wilson et al., 2008; Wilson
and Knoll, 2010; Wilson and Fischer, 2011).
This review will: 1) summarize the state of
knowledge on plant water transport; 2) describe
the models used to quantify this aspect of plant
performance; 3) outline some of the evolutionary
patterns that result from application of these
models to the fossil record; and 4) sketch out
future directions and applications of plant
physiological evolution.
Part 1: How do plants work?
At the core of terrestrial plant metabolism are
a series of tradeoffs that drive the radiation of
plant form and function (Niklas, 1994, 1997). One
of the most important tradeoffs is the loss of water
(in the form of water vapor) in exchange for the
acquisition of carbon dioxide from the
atmosphere (Taiz and Zeiger, 2002). In order to
acquire carbon dioxide as a substrate for
photosynthesis, plants expose their water-rich
interior tissues to the dry atmosphere, leaving
plants at risk of lethal desiccation. Plants have
evolved a series of tissues to transport water from
the soil to the sites of gas exchange, collectively
called xylem, along with a second system to
deliver photosynthate from leaves throughout the
rest of the plant, called phloem.
Xylem forms a network of hollow tubes from
the roots to evaporative surfaces, and flow
through xylem is driven by evaporation of water
from cells in the interior of leaves. As water is
evaporated from the cell walls, surface tension
causes small menisci (radius of curvature: ~10 to
50 nm) to form between cellulose microfibrils
(~20 nm in diameter). With increasing
In Ecosystem Paleobiology and Geobiology, The Paleontological Society Short Course, October 26, 2013. The
Paleontological Society Papers, Volume 19, Andrew M. Bush, Sara B. Pruss, and Jonathan L. Payne (eds.).
Copyright © 2013 The Paleontological Society.
THE PALEONTOLOGICAL SOCIETY PAPERS, VOL. 19
FIGURE 1.—Detailed view of xylem anatomy and pit structure in Paleozoic plants. B–E modified from Li and
Taylor (1999). A) Longitudinal section of xylem in the stem group lycophyte Asteroxylon mackei (Early Devonian,
Rhynie Chert) showing annular thickenings, modeled using scalariform shapes in Wilson and Fischer (2011). B)
Cross-section of a stem of the gigantopterid climbing plant Vasovinea tianii (late Permian, Xuanwei Formation),
arrows indicate gaps that could be missing medullary rays; note the wide xylem vessels. C) Scanning electron
micrograph of the specimen pictured in B); arrows indicate oblique endwalls, characteristic of vessels. D) A radial
view of a vessel endwall in Vasovinea tianii showing a multiperforate perforation plate (pp). E) Tangential view of
the perforation plate of a gigantopterid vessel; note enormous width of the gigantopterid vessel. F) Radial view of
secondary xylem in Cordaites sp. (Pennsylvanian stem group conifer) showing clusters of circular-bordered pits and
narrow tracheids. G) Radial view of clusters of circular-bordered pits on the secondary xylem of the
progymnosperm Callixylon newberryi (Archaeopteridiales; Late Devonian). Specimen courtesy of Jean Galtier and
Brigitte Meyer-Berthaud. H) Radial view of narrow tracheids in the stem group seed plant Medullosa anglica
showing abundant circular-bordered pits (Pennsylvanian, Shuler Mine, Harvard University Paleobotanical
Collection #24474).
2
WILSON: MODELING EVOLUTION OF PLANT HYDRAULICS
evaporation, more water is lost from cell walls
and the radius of curvature of the menisci
decreases; the strong surface tension and
hydrogen bonding of water molecules generates,
in turn, a tension, or negative pressure, that draws
water to the site of evaporation. This mechanism,
combining evaporation, surface tension,
hydrophobic cell wall compounds in xylem, and
hydrogen bonding between water molecules, is
described as the Cohesion-Tension Theory and
results in the movement of water to the tops of the
tallest trees without the expenditure of ATP
( D i x o n a n d J o l y, 1 8 9 5 ; D i x o n , 1 9 1 4 ;
Zimmermann, 1983; Tyree and Sperry, 1988;
Tyree and Ewers, 1991; Pockman et al., 1995;
Sperry et al., 1996; Tyree and Zimmermann,
2002; Wheeler and Stroock, 2008). Xylem
efficiency can be assessed with economic
comparisons: all costs to the plant are involved
with construction and maintenance, so if these
costs are equal, then the highest flow rate is the
most efficient.
As a result of the passive nature of water
transport in xylem, the anatomy and structure of
xylem cells determine the relative ease or
difficulty of water transport through plants. That
is, the dimensions, frequency, orientation, and
morphology of transport cells determine the
resistance to flow that water experiences on its
way through a plant: the driving force,
evaporation from the leaves, will vary throughout
the day, but the hydraulic architecture of the
transport system remains constant. Therefore,
assessing the hydraulic resistance of the vascular
system yields insight into the ecological and
physiological characteristics of a plant
independent of environmental variation. This
method can be particularly useful in deep time,
when even the most basic environmental
parameters (e.g., atmospheric CO2 concentration)
can be underdetermined (Royer, 2006).
Among vascular plants, xylem cells fall into
one of two broad categories: single-celled
tracheids, typically found in lycophytes (Fig. 1A),
ferns, and gymnosperms (Fig. 1F–H); and
multicellular vessels, formed from individual cells
called vessel elements, which reach their peak of
diversity in the angiosperms but have been
discovered in extinct lineages (Fig. 1B–E). Both
vessels and tracheids have a number of
morphological features in common: they are dead,
empty cells that are differentiated, in a
developmental sense, from parenchyma
procambial cells; both are roughly tube-shaped;
and both have a series of porous features on their
lateral walls to permit water to move from one
cell to another, called pits (Fig. 2C–F, H).
However, vessels and tracheids typically have a
dramatically different aspect ratio. Vessel
elements range from ~20 to more than 500
microns in diameter, 0.5–2 mm long, and are open
at the top and bottom, but, when stacked, form
multicellular vessels that can be several meters
long (Tyree and Ewers, 1991; Fisher et al., 2002).
Tracheids, on the other hand, are usually 5–35
microns in diameter, 1–5 mm long, and closed at
both ends, forming woody tissue that is composed
of a large number of small, closed cells.
By employing vessels and tracheids to
provide a low-resistance pathway to the leaves,
the cohesion-tension system can be highly
efficient. However, the cohesion-tension system
of water transport has its drawbacks. The most
pervasive drawback is the threat of a water
column rupture. Because the column is under
tension, it is metastable: mechanical failure,
pathogen activity, excessive drought, or
environmental disturbance can allow air to
penetrate the exterior of a plant and enter the
transpiration stream. When air bubbles enter the
transpiration stream, or the water column breaks
under extreme tension, air bubbles will expand
and fill the conduit, blocking transport of water
(Tyree and Sperry, 1989). The nucleation of an air
bubble or its entry into a xylem cell is called
cavitation, and the expansion of the air bubble to
block the conduit is called embolization. Unless
the plant grows new xylem cells or reverses the
embolism, flow through that conduit will stop,
photosynthesis will halt, and the plant will die.
A variety of observations have pointed toward
pit membrane morphology, architecture, and
frequency as key factors determining vulnerability
to cavitation and embolism; one of the most
compelling has been documenting differential
cavitation vulnerability in plants with similar
xylem cell sizes but different pits (Sperry et al.,
2002, 2005, 2006, 2007; Wheeler et al., 2005;
Hacke et al., 2006, 2007; Pittermann et al., 2006a,
b). These observations have shown that cavitation
vulnerability is more strongly determined by pit
structure than by any other single factor. The
standard pit membrane is a permeable sheet of
cellulose microfibrils, a remnant of the primary
cell wall between two developing xylem cells
(Fig. 2C, D). This type of membrane is often
called a homogeneous pit membrane, containing
small pores between the cellulose microfibrils on
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THE PALEONTOLOGICAL SOCIETY PAPERS, VOL. 19
FIGURE 2.—Xylem anatomy of living and extinct
plants. A) Cross-section of Medullosa anglica,
showing extremely wide tracheids in the primary and
secondary xylem (Pennsylvanian, Harvard University
Paleobotanical Collection #7791). B) Cross-section of
the sphenopsid Sphenophyllum insignis containing
very large diameter tracheids and crushed primary
xylem cells in the center (Pennsylvanian, HUPC
#29234). C) A close-up view of a circular-bordered pit
membrane from a fusainized tracheid of Callixylon sp.
(Early Mississippian; modified from Beck et al., 1982).
D) A radial view into pit membrane apertures of
tracheids from Medullosa sp.; note the dramatic
difference in size from the previous pit (Pennsylvanian,
Shuler Mine). E) Radial view of an elliptical/
scalariform pit from an extant vesselless angiosperm,
Trochodendron araloides (modified from Hacke et al.,
2007). F) Radial view of fusainized tracheids of
Callixylon sp. (Early Mississippian) showing a single
row of circular-bordered pits; this bears a close
resemblance to the arrangement of pits in most extant
conifers (modified from Beck et al., 1982). G) Radial
view of macerated tracheids of Medullosa sp.; note the
abundance of circular-bordered pits and the dimensions
of the two cells (Pennsylvanian, Shuler Mine). H)
Radial view of a torus-margo pit from the loblolly
pine, Pinus taeda (modified from Côte, 1967).
the order of 5–40 nm in diameter (Choat et al.,
2003, 2006; Choat and Pittermann, 2009). When
the aperture around the pit is circular, the entire
pit is called a circular-bordered pit (Fig. 2C, D);
this is the most common pit morphology. When
the aperture around the pit membrane is
elliptically shaped, the pit is known as a
scalariform pit (Fig. 2E). These are found in a
wide variety of spore-bearing plants, in the
primary xylem of many seed plants, and on some
angiosperm vessels. In some plants, the aperture
remains circular, but the pit membrane
differentiates into a thickened central portion and
a very porous outer margin, known as the torus
and margo, respectively (Fig. 2H). These torusmargo pits have the benefit of a high porosity
because of the large pores in the margo (100–
1000 nm in diameter), and a high safety margin,
because the thickened torus can seal off the pit
aperture in the event of embolism, acting as a
valve to prevent the spread of air from one cell to
another. The torus-margo pit is a key innovation
within the conifer lineage and Ginkgo, and it
appears to have evolved several times (Tyree and
Sperry, 1989, 2003; Pittermann et al., 2005,
2006a; Sperry et al., 2006).
Until recently, embolism was thought to be
irreversible, and damage from cavitation was
thought to be mitigated by the production of new
xylem cells (Zimmermann, 1983; Tyree and
Sperry, 1989). However, a series of observations
made over the last decade has shown that some
plants possess the ability to refill embolized
conduits when supplied with more water. In one
experiment, MRI imaging of an actively
transpiring stem of grapevine (Vitis vinifera)
showed a reduction in the number of embolized
vessels over a period of hours when the roots
were supplied with additional water (Holbrook et
al., 2001). Further investigation has shown that
refilling is a dynamic process involving active
transport of water from neighboring living cells
into embolized conduits, suggesting that sugars
and other solutes play key roles in this process
(Holbrook et al., 2001; Clearwater and Goldstein,
2005; Brodersen et al., 2010; Secchi and
Zwieniecki, 2011, 2012; Totzke et al., 2013). It
appears that a high frequency of living cells
within the xylem is a necessary precondition for
embolism refilling, but it may not be a sufficient
condition.
The great benefit of these plant physiological
discoveries is that the 400 Ma paleontological
record of fossil xylem can be subjected to
quantitative analysis. Both xylem cell
morphology (Fig. 2A, B) and pit membrane
structure (Fig. 2C–E) can be preserved in the
fossil record. From these dimensions, hydraulic
resistance and ecological characteristics of extinct
plants can be quantified. Earlier work focused
exclusively on xylem cell length and diameter
4
WILSON: MODELING EVOLUTION OF PLANT HYDRAULICS
(Niklas, 1985; Cichan, 1986a), but more recent
work has included pit structure on the resistance
side and cavitation resistance on the drawback
side (Wilson et al., 2008; Wilson and Knoll, 2010;
Wilson and Fischer, 2011).
Part 2: Quantifying flow rates
How can these key physiological parameters
be quantified? Many of the quantitative
observations of the effects of differential plant
anatomy on transpiration rates were made by I. W.
Bailey and colleagues during the 20th century
(Bailey and Thompson, 1918; Bailey and Tupper,
1918; Bailey, 1953). The quantitative foundations
for the mathematical model described here were
laid by a variety of laboratories (Lancashire and
Ennos, 2002; Hacke et al., 2004; Sperry and
Hacke, 2004). Detailed descriptions of parameters
and derivations can be found in previous work
(Wilson et al., 2008; Wilson and Knoll, 2010;
Wilson and Fischer, 2011).
The first quantitative breakthrough for
mathematical modeling of hydraulic resistance,
published by van den Honert (1948), applied the
analogy of the flow of current through an
electrical circuit of a defined electrical resistance
to the flow of water through a plant with a defined
hydraulic resistance. This relationship was
expressed by using an analogy to Ohm’s Law, in
which the flow of current across a circuit (I) is
defined by the electrostatic potential difference
(ΔV) divided by the electrical resistance (R):
I = ΔV / R
(Eq. 1)
Using the Ohm’s Law analogy, the flow of water
through a plant (Q) is defined by the pressure
drop across the plant (ΔP) divided by the
hydraulic resistance (R):
Q = ΔP / R
(Eq. 2)
In this analogy, environmental variation
(including relative humidity and temperature) has
strong effects on the pressure gradient, which will
change dramatically throughout the day. However,
the hydraulic resistance is unchanging and is a
function of anatomical properties of the xylem.
This analogy could be applied to an entire plant
(pressure drop from leaf to soil; equations
summing up the hydraulic resistance of the entire
path length from root to leaf), but to facilitate
comparison between different plants, particularly
fossil plants that may not be understood as entire
organisms, this analysis is best done on a singlecell scale.
Looking at a single xylem cell allows the total
hydraulic resistance (Rtot) to be deconvolved into
two parts: hydraulic resistance from flow through
the center of the xylem cell, the lumen (Rlumen),
and hydraulic resistance from flow into and out of
that cell through two sets of anatomical structures
called pits (Rpit):
Rtot = Rlumen + 2 (Rpit / Npit)
(Eq. 3)
Xylem cells are approximately cylindrical in
shape; therefore the hydraulic resistance of flow
through the lumen can be approximated using the
Hagen-Poiseuille equation, which is strongly
determined by the diameter of the tube (D) but
also includes parameters for tube length (L) and
viscosity of water (νH2O). Experimental studies
have shown that the average molecule of water
traverses half of the length of the cell before
moving into the next cell, and substituting this
distance (0.5 * L) for length into the standard
Hagen-Poiseuille equation results in the following
equation:
Rlumen = (64 νH2O L) / π (Dtracheid)4
(Eq. 4)
Pit structure is more complex, with each xylem
cell containing numerous pits and each pit
containing two morphological features: an
opening called an aperture and a porous sheet
called a membrane. As described above, pit
apertures and membranes vary dramatically
across terrestrial plants, and three types are very
common: circular-bordered pits (Fig. 2C, D),
which have a roughly circular aperture
surrounding a thin membrane; scalariform pits,
which are more elliptical in plan view (Fig. 2E);
and torus-margo pits, which have a circular
aperture surrounding a membrane that has
differentiated into an outer, porous portion (the
margo) and an impermeable, inner portion (the
torus) that can move back and forth and act as a
valve (Fig. 2H).
Pits are modeled as resistors in parallel. That
is, an increase in the number of pits (Npit) yields a
decrease in the total hydraulic resistance of that
particular xylem cell: with more pits, water moves
easily from one xylem cell to another (Eq. 3). In
most vascular plants, two pits are aligned with
one another in adjacent cells and water flows
from one to another; these structures are called pit
pairs. Each pit’s hydraulic resistance has a
5
THE PALEONTOLOGICAL SOCIETY PAPERS, VOL. 19
FIGURE 3.—A quantitative comparison of living and extinct plant water transport capabilities using modeled (left
panel) and experimental (right panel) hydraulics values, from Wilson et al. (2008). On the left are results from
twelve model runs, four each from Medullosa, the stem group conifer Cordaites, and the living conifer Pinus. Each
point represents a model run for conductivity of a single tracheid normalized to length and wall area of the cell
(conduit-specific conductivity). At each point, a particular value for pit-area resistivity (pit resistance normalized to
pit area; rp) is substituted into the model, showing how different pit membrane porosities can be simulated; bold
values are rp values that satisfy the 80-20 (vessel) or 60-40 (tracheid) pit-lumen resistance partitioning. On the right
are single-conduit values for hydraulic conductivity from an angiosperm vessel, a tracheid-bearing angiosperm that
has secondarily lost vessels, and a conifer. rp values are also pit resistance values; numbers are conduit diameters.
Medullosan tracheids have substantial overlap with the hydraulic space that angiosperm vessels occupy.
component derived from each aperture of the pit
pair, determined by aperture morphology
(Raperture), and another component derived from pit
membrane morphology and porosity (Rmembrane):
Rpit = Rmembrane + 2 Raperture
(Eq. 5)
Pit apertures are modeled as short, cylindrical
openings using a slightly modified HagenPoiseuille equation (compare with Eq. 4) that
includes the aperture diameter (Dap) and thickness
(tap):
Raperture = [128 tap νH2O / π (Dap)4 ]
+ 24 νH2O / (Dap)3
(Eq. 6)
Whereas pit membranes are modeled as thin,
cylindrical sheets with pores of defined diameter
(Dpore) and number (Npore):
Rmembrane = 24 νH2O / Npore (Dpore)4
(Eq. 7)
Pit membrane porosity is among the most
important parameters in this analysis. Pit
membrane pores are very small: they are typically
5–20 nm in diameter for circular-bordered pits
and scalariform pits, with pores infrequently
reaching diameters in excess of 200 nm (Choat et
al., 2003; Jansen et al., 2009), but can be more
than 1 micron in diameter in torus-margo pits
(Fig. 2H) (Côte, 1967). It is this difference in pit
membrane pore size that allows conifers to match
the hydraulic efficiency of angiosperms on a perxylem-area basis (Pittermann et al., 2005, 2006,
2010).
Using this mathematical model, the
contribution of pit membrane pores can be
modeled using a variety of statistical distributions
of pore sizes: normal distributions have been used
6
WILSON: MODELING EVOLUTION OF PLANT HYDRAULICS
(Wilson et al., 2008), but substituting alternative
distributions of sizes is trivial. A series of
simulations of the effect of different pit membrane
porosities based on different values of pore
membrane diameters are shown for the stemgroup seed plant Medullosa, the stem-group
conifer Cordaites, and the living conifer Pinus in
Figure 3. In the left panel, the hydraulic
conductivity for tracheds from these three genera
are shown, along with the effect of different pit
membrane porosities (expressed as pit area
resistance: pit resistance normalized to pit
membrane area, or rp) on the total hydraulic
conductivity of each cell. As pits become less
resistant, the hydraulic conductivity increases.
When these modeled values are compared with
hydraulic conductivity values derived from
single-cell hydraulic resistance experiments on
angiosperm vessels, conifer tracheids, and
vesselless angiosperms (Fig. 3, right panel),
medullosan tracheids are found to occupy the
same hydraulic space as angiosperm vessels, and
both Pinus and Cordaites closely overlap
experimental values from conifer tracheids
(Wilson et al., 2008).
In order to constrain values for pit membrane
porosity, it is necessary to rely on guidelines
derived from experimental data on living plants.
When the proportion of hydraulic resistance
coming from pits and pit membranes has been
measured in living plants, small conduits (both
tracheids and small vessels) have 54–60% of their
hydraulic resistance arising from pits, whereas
large conduits have 80–87% of their resistance
arising from pit number and structure (Sperry et
al., 2005; Wheeler et al., 2005; Choat et al.,
2006). Xylem cells with large diameters have a
lower Rlumen, increasing the other component of
hydraulic resistance, that from pits and end walls.
These relationships between lumen resistance and
end-wall resistance can be used to evaluate and
constrain parameters in these models, especially
pit membrane porosity: in most plants, Rlumen
would be expected to make up ~10–50% of the
total hydraulic resistance, and pit membrane
porosity can be adjusted accordingly.
When Equations 1 through 7 are examined, it
should be clear that all of the terms used fall into
one of four categories: 1) empirically measurable
directly from fossilized material (e.g., Dtracheid,
D a p ) ; 2) exhibiting limite d but k n o wn
environmental variation (e.g., νH2O); 3) constants;
or 4) spanning a range of sizes known from living
specimens, but testable using sensitivity analysis
(e.g., Dpore). Taken together, a series of descriptive
relationships emerge from these equations
(Wilson and Knoll, 2010) as follows:
1) Wider cells have a lower hydraulic
resistance and are more efficient.
2) Pit membrane resistance is the next most
important parameter.
3) Length is the third-most important
parameter as a linear term in the model.
Some useful dimensions and comparative
hydraulic data can be found in Table 1.
Finally, the total hydraulic resistance (Rtot)
can be expressed in a more intuitive form as its
inverse, hydraulic conductance (K), which is
simply the inverse of resistance. Hydraulic
conductance can be normalized to any of several
dimensions to yield hydraulic conductivity,
including cell length, lumen area, pit area, or wall
volume (Comstock and Sperry, 2000). Overall,
low hydraulic resistance translates into high
hydraulic conductance or conductivity, and vice
versa.
Part 3: Quantifying drawbacks: cavitation and
embolism resistance
The mechanism of cavitation and embolism
points toward ways in which anatomical variation
can be used to predict relative vulnerability. Low
xylem pressure (or high tension) can draw air
through pores in pit membranes, or around
imperfectly sealed tori in conifer tracheids,
pulling air into the transpiration stream (Cochard
et al. 2009; Delzon et al. 2010). Therefore, in
some way, pit-membrane pore diameter, along
with the number of pits, size of pits, and/or
dimensions of pit membrane area, should be
predictive for embolism resistance (Hacke et al.,
2001, 2007, 2007; Sperry et al., 2005; Wheeler et
al., 2005; Pittermann et al., 2006a; Hacke and
Jansen, 2009). Observations on living plants, both
vessel-bearing and tracheid-bearing, largely bear
out a relationship between increased pit area and
increased cavitation vulnerability (Wheeler et al.,
2005; Christman et al. 2012), but caution should
be used when interpreting these estimates because
there are uncertainties regarding the strength of
these observations (Christman et al., 2009).
Furthermore, statistical relationships based on one
taxonomic group do not normally hold when
applied to other taxonomic groups: high pit
membrane area on a fern tracheid is much greater
than high pit membrane area in a conifer tracheid.
The simplest method for calculating the
likelihood of air-seeding and cavitation relies on
7
THE PALEONTOLOGICAL SOCIETY PAPERS, VOL. 19
TABLE 1.—Key physiological parameters and morphological features for extinct and extant plant xylem. Key
references for measured values and ranges include: Diameter: Bailey and Tupper, 1918; Bannan, 1965. Length:
Bailey and Tupper, 1918; Bannan, 1965. Pit Membrane Pore Diameter: Côte, 1967; Choat et al., 2004, 2008; Rabaey
et al., 2006; Sano and Jansen, 2006; Jansen et al., 2007, 2009. Air-seeding Pressure: Sperry, 1986; Sperry and Tyree,
1988, 1990; Sperry et al., 1994, 2005, 2006, 2008; Hacke et al., 2000, 2001a; Hacke and Sperry, 2001; Pittermann
and Sperry, 2003, 2006; Domec et al., 2006, 2008, 2009; Pittermann et al., 2006a; Johnson et al., 2013. Implosion
Pressure: Hacke and Sperry, 2001; Hacke et al., 2001a; Sperry, 2003; Cochard et al., 2004; Domec et al., 2006,
2008, 2009; Johnson et al., 2013.
Name
Age
Angiosperm
vessels
Extant
Vessel
elements
Extant
Conifer
tracheids
Extant
Pit
membrane
Diameter Length Pit membrane
pore
(µm)
(mm)
type
diameter
(nm)
Homogeneous,
scalariform or
10–
5–40
20–500
circular10,000
bordered
Homogeneous,
scalariform or
5–40
20–500 0.5–2
circularbordered
5–40
1–5
Torus-margo
~330– 252 Ma
Homogeneous,
1.5–5
circular(Mississippian 15–45
bordered
to late Permian)
~330–295 Ma
Homogeneous,
(Mississippian
10–30
30–250
circularMedullosa
to early
(or more)
bordered
Permian)
Homogeneous,
404 Ma (Early
scalariform to
Asteroxylon
13–34 0.9–2.4
Devonian)
helical/annular
(“G-type”)
Cordaites
an equation for air passing through a pore in a
membrane—in this case, for air passing through a
pore in the pit membrane of a given size (typically
5–40 nm). The pressure gradient (ΔP) in MPa
required to pull a bubble through a pore of a given
diameter (Dpore) is a function of the surface
tension of water (τ) and the contact angle between
water and the pit membrane (θ; assumed to be 0°):
ΔP = 4 (τ cos θ / Dpore)
(Eq. 8)
Substituting modeled pore dimensions allows the
cavitation pressure of individual pit membranes
(and therefore xylem cells) to be quantified.
Based on dimensions mentioned in the
previous section, a pit membrane with uniformly
AirImplosion
seeding
pressure
pressure
(MPa)
(MPa)
-1 to -8
-3 to >-10
100–1000
-1 to -7
-2.5 to >-10
5–40
-4 to -7
-5 to -9
5–100
-0.8 to -2
-2 to -3
5–40
-2 to -5
-6 to -8
distributed pores the size of those found in the
margo of torus-margo pits (100–1000 nm) would
be extremely vulnerable compared with those
found in homogeneous pit membranes (5–20 nm,
occasionally reaching 50 nm). However, in
conifers and Ginkgo biloba, which bear torusmargo pits, the valve action of the torus, coupled
with additional thickening of the margo fibers,
prevents the spread of embolism, although
repeated air-seeding events can increase the
likelihood of a tear in the margo, allowing the
torus to slip out of place—a phenomenon known
as cavitation fatigue (Sperry and Tyree, 1988,
1990; Sperry and Sullivan, 1992; Hacke et al.,
2001).
Along with pit membrane rupture and tearing,
8
WILSON: MODELING EVOLUTION OF PLANT HYDRAULICS
another type of permanent, irreversible damage
can occur: under extreme drought conditions,
water-column tension can be so great that it
collapses the xylem cells, leading not only to
embolism but to conduit collapse (Hacke et al.,
2001). Implosion is a common problem in biofuel
crop strains that have been engineered to produce
low amounts of the biopolymer lignin. In these
plants, the xylem cells are not rigid enough to
withstand the mechanical forces of a transpiration
stream under extreme tension, and the cells
collapse, cutting off the water supply to the
leaves, with lethal results (Wagner et al., 2009).
Implosion, therefore, is the extreme state of
drought stress beyond cavitation and embolism,
and quantifying implosion resistance permits
robust estimates of a plant’s physiological limits:
they cannot be expected to live where their xylem
would implode. Fortunately for paleobiologists,
implosion pressure (I) is largely conveyed by the
architecture of xylem cells themselves,
specifically the square of the ratio of radial
double-wall thickness (t) to the lumen diameter
(b) of the xylem cell (Hacke et al., 2001). Cells
with wide lumens and relatively thin walls are
more vulnerable to implosion than cells with
narrow lumens and thick walls, and statistical
relationships have been derived through
experimentally induced implosion (Hacke et al.,
2001) (Table 1).
I = (t / b)2
(Eq. 9)
Both lumen width and cell wall thickness are easy
to measure in cross-sections of fossil plant wood,
and these measurements yield important
physiological results (Fig. 1).
One caveat should be added to this analysis:
the vast majority of the experimental work on
xylem function has been aimed at understanding
vessel and tracheid function. Specifically, it has
been aimed at understanding conduits with
normal dimensions, and the statistical
relationships derived from this experimental and
modeling work is at its most accurate and precise
when dealing with this portion of the parameter
space. When dealing with unusual tracheid
features (especially very high or low length or
width and/or very high or low pit frequencies), an
extreme result should be viewed as an indication
that the particular xylem cell in question is
outside of the statistical distribution defined by
extant plants. For example, medullosan tracheids
are so extreme in their length and width that they
have a very low value for Rlumen. When typical
pit-membrane pore dimensions (5–20 nm) are
used, the pits account for 98% or more of the
hydraulic resistance of the cell. This is not out of
the realm of possibility: the vessels within the
American elm (Ulmus americana) have
approximately 87% of their hydraulic resistance
coming from pits (Choat et al., 2006). However,
when choosing between model parameters, it is
good practice to approach existing hydraulic
allometries to as close a degree as possible. In the
case of Medullosa, this means expanding the pit
membrane pore size range to 5–100 nm to restore
the lumen-pit balance to approximately 8 to 92%.
Part 4: Patterns and trends
When the fossil record of vascular plants is
viewed through the lens of water transport,
several observations and patterns come into focus.
First and foremost, the angiosperm vessel and
torus-margo pit in gymnosperms are key
innovations, as other authors have noted over the
last one hundred years (Bailey and Thompson,
1918; Bailey and Tupper, 1918; Bailey, 1953;
Tyree and Ewers, 1991; Tyree and Zimmermann,
2002; Pittermann et al., 2005; Hacke et al., 2006,
2007; Sperry et al., 2006, 2007, 2008; Feild et al.,
2009; Pittermann, 2010; Feild and Wilson, 2012).
Both vessels and torus-margo pits dramatically
reduce the hydraulic resistance in seed plants;
torus-margo pits have the added advantage of
providing increased safety through the action of
their valves, so vessels can afford the increased
hydraulic resistance and safety margin of
homogeneous pit membranes (relative to torusmargo pits) because of their dramatically reduced
lumen resistance. But, when vessels and torusmargo pits are placed into their evolutionary
context, they are only two of the strategies that
plants have explored to increase hydraulic
efficiency. These other strategies are depicted
stratigraphically in Figure 4, but can be broken
down into three patterns.
Pattern 1: High hydraulic conductivity
evolved many times.—The most obvious pattern
that becomes clear when looking at the hydraulic
capabilities of fossil plants is that plants have
evolved many strategies to achieve high hydraulic
conductivity (Fig. 4, red, pink, and orange bars).
As described in previous work (Wilson and Knoll,
2010), there are a variety of extinct plants that
achieved relatively high conductivity through
either decreasing lumen resistance (i.e.,
developing larger conductive cell diameters) or
9
THE PALEONTOLOGICAL SOCIETY PAPERS, VOL. 19
FIGURE 4.—Stratigraphic ranges of plant groups coded for their hydraulic adaptations. Stratigraphic ranges and
taxonomic names are from Taylor et al. (2008), with the exception of the fiberless angiosperms, used here to
describe Early Cretaceous angiosperm flora of primarily small flowering plants that did not produce fibers from
their vascular cambium (Philippe et al., 2008). ANITA corresponds to the eight basal angiosperm families
(Amborellaceae, Nympheaceae, Illiciaceae, Trimeniaceae, Australbaileyaceae, Cabombaceae, Hydetellaceae,
Schisandraceae). Colors represent some adaptations discussed in the text: scalariform pits, torus-margo pits, large
tracheids, increased pit frequencies, and vessels. Large tracheids (red bars) are common in stem-group seed plant
groups (Medullosa, Lyginopteris, Callistophyton, Calamopityales) and Sphenophyllum (red bar within sphenopsids);
vessels (pink bars) evolve independently in the gigantopterids, the seed-plant group Gnetales, and in the roots of the
polypod ferns (and possibly in other fern groups; Carlquist and Schneider, 2007); torus-margo pits (orange bars)
evolve late within the conifer clade (and Ginkgo); scalariform pits (green bars) are the most common xylem type in
spore-bearing plants. A vessel- and torus-margo-dominated world is a Cenozoic phenomenon.
decreasing wall resistance (i.e., adding more pits
or decreasing the resistance of individual pits).
A number of extinct plants even pursued both
strategies: evolving wide, long conduits with
many pits. These plants tend to be smaller in
stature, subcanopy or climbing, and have a
moderate to high ratio of leaf-area to secondaryxylem area. These include the Paleozoic seed
plants Lyginopteris, Medullosa, and
Callistophyton, and the climbing sphenopsid
Sphenophyllum; and the Mesozoic seed plant
Pentoxylon. Each of these plant groups evolved
tracheids more than 80 microns in diameter;
Medullosa (Fig. 1H; 2A, D, G) and
Sphenophyllum (Fig. 2B) contain both the longest
and widest tracheids described to date in the fossil
record, often exceeding 250 microns in diameter
and 25 mm (2.5 cm) in length—roughly ten times
10
WILSON: MODELING EVOLUTION OF PLANT HYDRAULICS
wider and longer than typical seed-plant tracheids
(Andrews, 1940; Delevoryas, 1955; Cichan and
Taylor, 1982; Cichan, 1985, 1986b, c; Wilson et
al., 2008; Wilson and Knoll, 2010). Precisely how
these two plant groups managed to develop cells
of such extraordinary size is something of a
developmental mystery, but unusual activity of
the vascular cambium and a high degree of
internodal elongation are likely to be the cause
(Cichan, 1985, 1986b, c).
One consequence of the enormous tracheids
found in Medullosa and Sphenophyllum is that
these cells reach heights of hydraulic conductivity
that terrestrial plants do not reach again until the
evolution of angiosperm vessels during the
Cretaceous (Feild and Wilson, 2012). Medullosan
tracheids, in particular, are functionally
indistinguishable from some crown-group
angiosperm vessels (Wilson et al., 2008). Where
these enormous tracheids diverge from
angiosperm vessels, however, is in cavitation
resistance: both medullosan tracheids (Wilson et
al., 2008) and tracheids of Sphenophyllum (J.
Wilson, unpublished data) are extraordinarily
vulnerable to cavitation from their high pit area.
The large lumens and relatively thin cell walls
found within Medullosa and Sphenophyllum make
them vulnerable to implosion at relatively modest
tensions as well: the largest tracheids in each plant
could implode at tensions as low as –2 MPa, a
value temperate plants tolerate on a warm, dry,
sunny day.
Large tracheids are extremely rare among
living plants, with one reported occurrence in the
climbing fern Salpichlaena volubilis, found in
Central American tropical forests (Veres, 1990;
Giudice et al., 2008; Luna et al., 2008). It is
possible that other climbing ferns, including
common genera such as Gleichenia, may include
specimens with similarly wide or long tracheids—
a number of authors have made similar
observations in passing (e.g., Bliss, 1939).
Pattern 2: Safety last—An evolutionary
pattern that is found in both seed plants and sporebearing plants is that adaptations to increase
hydraulic conductivity precede adaptations to
increase water transport safety. Relatively
evolutionarily early plants contain adaptations
that maximize hydraulic conductivity and are
replaced or succeeded by plants with safer xylem.
The most obvious example of this pattern
comes from comparing extinct and extant
conifers. Early conifers, including both stemgroup conifers, such as Cordaites (Fig. 1F), and
extinct members of crown-group conifer clades,
all contain tracheids with a higher number of
circular-bordered pits on their lateral walls than
extant conifer species; all living conifer groups
contain torus-margo pits instead (Fig. 4; blue and
orange bars). In fact, the earliest torus-margo pit
in conifers does not appear until the Hettangian
(Early Jurassic, ~200 Ma) (Philippe and Bamford,
2008). When the cavitation vulnerability of these
two adaptations is compared (multiple circular
bordered pits vs. torus-margo pits), the stemgroup conifers are more vulnerable to cavitation
through the increase in pit area (Wilson and
Knoll, 2010). To put it another way, ecologically
successful conifer lineages with multiple circular
bordered pits have all been replaced by
ecologically successful conifer lineages with
safer, fewer, higher-conductive torus-margo pits.
This pattern is also seen when looking at
scalariform pits (Fig. 4, green bars). The earliest
vascular plants contained a number of complex
structures on their xylem cell walls, including
some features that are so ambiguous that it is
difficult to determine the degree to which these
apertures were porous at all (Graham and Gray,
2001; Edwards, 2003). However, these early
plants were succeeded by a number of vascular
plants that contained tracheids with scalariform
pits, which dramatically reduced the hydraulic
resistance of their vascular system but acquired an
increased risk of embolism. Psilophyton dawsonii
from the Early to Middle Devonian Battery Point
Formation on the Gaspé Peninsula, Canada,
contains xylem that is largely pit area and small
bars between pit membrane (Hartman and Banks,
1980). These cells bear a strong resemblance to
xylem from some modern ferns and metaxylem of
living seed plants, both of which are seldom longlived tissues. Particularly in small ferns, aerial
vegetative structures rarely persist more than a
year, and in seed plants, metaxylem’s functional
role is usually taken over by secondary xylem,
which tends to have a larger safety margin and is
more stable and long-lived. Psilophyton is not
singular: a number of other ancient lineages have
scalariform pits of varying sizes, including the
stem-group vascular plant Renalia, the ancestral
fern Rhacophyton, and the arborescent lycophytes
(Taylor et al., 2008). The early origin of
scalariform pitting and large wall areas devoted to
pit membranes implies an ecological strategy
among early terrestrial plants that is focused on
short-term gains: a ‘live fast, die young’ strategy
Pattern 3: Stem hydraulic adaptations radiate
11
THE PALEONTOLOGICAL SOCIETY PAPERS, VOL. 19
in step with leaves and roots—Over the last
several decades, it has become clear that
anatomical revolutions have taken place within
the terrestrial plant clade, including the evolution
of secondary growth (Scheckler, 1978; MeyerBerthaud et al., 2000), true rooting systems
(Raven and Edwards, 2001), laminar leaves
(Niklas, 1997), and the angiosperm leaf (Boyce et
al., 2009). It has been noted that each of these
transitions is associated with an increase in
vascularization and/or hydraulic efficiency
(Sperry, 2003), and single-cell analysis supports
this view (Fig. 4). The radiation of new
morphotypes and ecological strategies from the
Late Devonian through the Pennsylvanian is
accompanied by the evolution of large, efficient
tracheids in stem-group seed plants and
Sphenophyllum. Secondary xylem and the
appearance of laminar leaves evolve in step with
dense wood containing a number of circularbordered pits, as shown in Figures 1 and 2. The
large leaf areas of Carboniferous plants such as
Medullosa are hydraulically maintained by the
enormous tracheids found in stem-group seed
plants. The advent of angiosperms brings the rise
of angiosperm leaves along with vessels, and it is
a curious coincidence that the torus-margo pit
becomes the dominant pit structure in conifers at
approximately the same time.
Part 5: Outputs and horizons
The utility of mathematical models of plant
function is that informed estimates of plant
physiological properties can be derived from
fragmentary organs or disputed plants. For
example, the calamopityales are a plant group
known from permineralized, decorticated stems
found in Mississippian rocks across North
America and Europe, but leaves and reproductive
structures have not been discovered in organic
attachment to these stems (Rowe and Galtier,
1988; Speck and Rowe, 1994; Rowe et al., 2004;
Decombeix et al., 2005; Galtier and MeyerBerthaud, 2006; Decombeix et al., 2011a, b).
Calamopityalean plants are thought to be stemgroup seed plants because of the presence of
xylem containing large rays, an arrangement that
resembles other stem-group seed plants, including
Lyginopteris, Callistophyton, and Medullosa, but
until reproductive and foliar structures are
discovered, our knowledge of the anatomy and
phylogenetic position of these plants will remain
limited. However, when the hydraulic resistance
of these plants is calculated, a number of
calamopityalean species, including Calamopitys
embergeri (J. Wilson, unpublished data), occupy
the portion of the hydraulic morphospace later
explored by these other high-conductivity stem
group seed plants. Perhaps not surprisingly,
biomechanical analysis (Rowe et al., 1993) and
overall morphology (Galtier, 1970) of some of the
calamopityaleans has pointed toward lianescent or
non-self-supporting growth forms within this
group, whereas other species, including
Calamopitys schweitzeri, may represent
intermediate hydraulic strategies between conifers
and stem-group seed plants and may be selfsupporting (J. Wilson, unpublished data; Galtier et
al., 1993). Therefore, despite a limited window
into the whole-plant structure and anatomy of the
calamopityalean plants, inferences can be made
regarding their physiology and ecology.
As another example, gigantopterids are an
enigmatic group of plants known primarily from
foliar compressions from the Permian across Asia
and North America (Glasspool et al., 2004b;
Taylor et al., 2008). Permineralized specimens are
extremely rare, but demonstrate that some
gigantopterids contained leaf venation
comparable to that found in early angiosperms,
along with vessels in stems (Li et al., 1996; Li and
Taylor, 1998; Glasspool et al., 2004a, b; Boyce et
al., 2009). Within the permineralized stems of
gigantopterids, both vessels and tracheids can be
seen (Fig. 1B, C), and vessels can be
unambiguously distinguished by perforation
plates in plan (Fig. 1D) and transverse views (Fig.
1E). Although insights into gigantopterid stem
anatomy are limited because only a handful of
fossils contain preserved internal anatomy, if any
extinct plant were to occupy the physiological
ecospace later taken by early angiosperms, the
gigantopterids would be a strong candidate.
What may never be preserved?—Despite the
ecological insight gained from mathematical
modeling, key aspects of plant physiology may
never be preserved in the fossil record. For
example, embolism refilling appears to require
that living cells and vulnerable xylem cells be in
proximity so that living cells can pump solutes
into embolized conduits and redissolve the air
bubble under positive pressure (Clearwater and
Clark, 2003; Secchi and Zwieniecki, 2011, 2012).
Although there may not be a biochemical marker
for embolism refilling capacity that is preservable
over geologic time, the combination of vulnerable
conduits next to living ray cells or axial
parenchyma, with low amounts of secondary
12
WILSON: MODELING EVOLUTION OF PLANT HYDRAULICS
FIGURE 5.—Anatomy and morphology of Macroneuropteris scheuchzeri, a Pennsylvanian plant that presents a
physiological puzzle. A) Transverse section of a Medullosa noei stem, thought to produce M. scheuchzeri fronds.
Note three prominent xylem segments (each marked with a white x) in the center of the stem, surrounded by
multiple layers of periderm. Specimen courtesy of Tom Phillips. B) M. scheuchzeri specimen from Nova Scotia
showing heterophylly; from Zodrow (2003). C) Reconstruction of the frond architecture of a closely related species,
Macroneuropteris macrophylla, showing the basal bifurcation characteristic of many medullosan fronds. It is highly
likely that M. scheuchzeri fronds contained one more apical bifurcation. From Cleal et al. (1996).
xylem produced, may be read to imply refilling
capacity in fossil plant stems. Both Medullosa and
Pentoxylon meet these criteria, and some
calamopityalean species may as well.
Why the disconnect between leaves and
stems?—One of the puzzles among Paleozoic
seed plants is that a number of plants suggested to
have high hydraulic capacity also contain leaf
features that are normally interpreted as
xeromorphic: sunken stomata, a thick cuticle, and
abundant trichomes on the leaves. For example, in
the Pennsylvanian tropical forests of Pangea, the
medullosan plant Macroneuropteris scheuchzeri
(Fig. 5) contains these classic xeromorphic
features, yet facies analysis (i.e., environmental
reconstruction based on the sediments containing
these fossils) shows that Macroneuropteris
scheuchzeri occupied wetland environments,
rather than drier environments (Stull et al., 2012).
Furthermore, M. scheuchzeri leaves also contain
structures interpreted as hydathodes, secretory
tissues normally employed to excrete water from
the margin of leaves, which are normally found in
plants with access to an abundant water supply.
As Stull et al. (2012) pointed out, how can a leaf
contain both wet and dry features at the same
time, and why might these leaves be attached to a
low hydraulic resistance stem?
One possible way to reconcile this
discrepancy involves leaf crown scaling: if stemgroup seed plants, including medullosans, lacked
some of the leaf-level features to maximize
hydraulic efficiency seen in angiosperms,
including high vein density and rapidly
responding stomatal guard cells (Brodribb and
Holbrook, 2004; Brodribb et al., 2005, 2007,
2010; Brodribb and Feild, 2010; de Boer et al.,
2012), the massive leaf area found in many of
these plants may have placed steep demands on
the hydraulic supply by the stems. Stomatal guard
cells that responded slowly to changes in light
levels, temperature, soil water status, or humidity,
as found in lycophytes and ferns (Brodribb and
McAdam, 2011), may have led to high water loss
13
THE PALEONTOLOGICAL SOCIETY PAPERS, VOL. 19
from leaves, especially within plants that had a
large leaf area with leaves that may have persisted
over multiple years (Wnuk and Pfefferkorn, 1984;
Stull et al., 2012). If medullosan stomata reacted
to environmental stress as lycophytes and ferns
do, rather than the way most seed plants respond
(McAdam and Brodribb, 2012), hydathodes
would be advantageous when soil moisture
content was high, and the xeromorphic features
would be advantageous when environmental
conditions were dry. In effect, integrating slow
stomata over a large leaf area may only have been
possible with a low hydraulic resistance stem.
Simulating extinct ecosystems.—Finally, one
of the most promising directions this research can
take is to permit quantitative models of past and
future ecosystems based on individual plant
anatomy, including growth rates, water fluxes,
and carbon fluxes (Medvigy et al., 2009, 2010;
Hurtt et al., 2010; Ise and Moorcroft, 2010).
Mesoscale ecosystem models have been used to
model a variety of forest dynamics, from the
hydrologic feedbacks that perpetuate cloud forests
in Costa Rica to forest biomass dynamics under
high-frequency environmental variation (Medvigy
and Moorcroft, 2012). These models have
contributed substantially to resolving differential
spatial differences in predicted responses to
anthropogenic climate change (e.g., Medvigy et
al., 2010). Most of these models, including the
Ecosystem Demography 2 model (ED2)
(Moorcroft et al., 2001; Medvigy et al., 2009),
include multiple vegetation types, each with its
own biological properties, including growth rate,
transpiration rate, and crown size. The major
inputs to these models, therefore, can be resolved
from analysis of fossil plants, and it should be
possible to simulate past ecosystems, including
variability within ecosystems. For example, ED2
could be run to simulate both a lycophytedominated swamp and a medullosan-dominated
overbank ecosystem, and to explore their relative
contributions to the hydrologic cycle and
sensitivity to environmental conditions during the
Pennsylvanian. Not only would this contribute to
a more holistic understanding of these individual
ecosystems, but these ecosystems can then be
compared with modern analogues in a
quantitative way.
CONCLUSIONS
Applying mathematical models to fossil plant
material can provide a number of insights into
evolutionary trends in land plants. It appears that
early vascular plants prioritized low hydraulic
resistance over safety from embolism, a pattern
that is also seen within the conifer lineage.
Although the angiosperm vessel is the ultimate
low hydraulic resistance innovation among living
plants, a number of extinct plants (both seed
plants like Medullosa and at least one fern,
Sphenophyllum) evolved comparably efficient
xylem hundreds of millions of years before the
evolution of angiosperms. Future work will build
on these evolutionary patterns and will provide
quantitative data that can be used to create
accurate models of terrestrial ecosystems deep in
the geologic past, enriching our understanding of
the biological components of the Earth system.
ACKNOWLEDGEMENTS
Thanks to Andrew Knoll, Missy Holbrook,
Brendan Choat, Jim Wheeler, Brett Huggett, Todd
Dawson, Maciej Zweiniecki, Kevin Boyce,
Woody Fischer, Jarmila Pittermann, John Sperry,
Dana Royer, Bill DiMichele, Scott Wing, Herman
Pfefferkorn for discussion on various aspects of
this paper, but any errors or misperceptions are
the responsibility of the author. Rebecca Tobet
a n a l y z e d S p h e n o p h y l l u m ’s i m p l o s i o n
vulnerability as part of her senior thesis at
Haverford College. Special thanks to Jean Galtier,
Brigitte Meyer-Berthaud, Tom Phillips, Andrew
Knoll, and Suzanne Costanza for access to plant
fossils.
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